Neurons generated in senescence maintain capacity for functional integration

Hippocampus

Volumn 22, Issue 5, 2012, Pages 1134-1142

  Marrone, Diano F ^a,b,c   Ramirez Amaya, Victor ^d   Barnes, Carol A ^b,c  

^a WILFRID LAURIER UNIVERSITY   (Canada)

^b UNIVERSITY OF ARIZONA   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

^d INSTITUTO DE NEUROBIOLOGÍA   (Mexico)

Author keywords

Aging; Arc; Dentate gyrus; Neurogenesis

Indexed keywords

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL AGING; CELL POPULATION; CELL SURVIVAL; CONTROLLED STUDY; DENTATE GYRUS; GRANULE CELL; HIPPOCAMPUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

AGING; ANALYSIS OF VARIANCE; ANIMALS; BROMODEOXYURIDINE; CYTOSKELETAL PROTEINS; DENTATE GYRUS; HIPPOCAMPUS; LEARNING; MICROSCOPY, CONFOCAL; NERVE NET; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONAL PLASTICITY; NEURONS; RATS; RATS, INBRED F344;

EID: 84856455366     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20959     Document Type: Article

References (67)

1. Aimone JB, Wiles J, Gage FH. 2006. Potential role for adult neurogenesis in the encoding of time in new memories. Nat Neurosci 9: 723-727.
2. Aimone JB, Wiles J, Gage FH. 2009. Computational influence of adult neurogenesis on memory encoding. Neuron 61: 187-202.
3. Alme CB, Buzzetti RA, Marrone DF, Leutgeb JK, Chawla MK, Schaner MJ, Bohanick JD, Khoboko T, Leutgeb S, Moser EI, Moser MB, McNaughton BL, Barnes CA. 2010. Hippocampal granule cells opt for early retirement. Hippocampus 20: 1109-1123.
4. Ambrogini P, Cuppini R, Cuppini C, Ciaroni S, Cecchini T, Ferri P, Sartini S, Del Grande P. 2000. Spatial learning affects immature granule cell survival in adult rat dentate gyrus. Neurosci Lett 286: 21-24.
5. Bakker A, Kirwan CB, Miller M, Stark CE. 2008. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 319: 1640-1642.
6. Bizon JL, Gallagher M. 2003. Production of new cells in the rat dentate gyrus over the lifespan: Relation to cognitive decline. Eur J Neurosci 18: 215-219.
7. Bizon JL, Lee HJ, Gallagher M. 2004. Neurogenesis in a rat model of age-related cognitive decline. Aging Cell 3: 227-234.
8. Bramham CR, Alme MN, Bittins M, Kuipers SD, Nair RR, Pai B, Panja D, Schubert M, Soule J, Tiron A, Wibrand K. 2010. The Arc of synaptic memory. Exp Brain Res 200: 125-140.
9. Brunson KL, Baram TZ, Bender RA. 2005. Hippocampal neurogenesis is not enhanced by lifelong reduction of glucocorticoid levels. Hippocampus 15: 491-501.
10. Calhoun ME, Kurth D, Phinney AL, Long JM, Hengemihle J, Mouton PR, Ingram DK, Jucker M. 1998. Hippocampal neuron and synaptophysin-positive bouton number in aging C57BL/6 mice. Neurobiol Aging 19: 599-606.
11. Chawla MK, Guzowski JF, Ramirez-Amaya V, Lipa P, Hoffman KL, Marriott LK, Worley PF, McNaughton BL, Barnes CA. 2005. Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience. Hippocampus 15: 579-586.
12. Clelland CD, Choi M, Romberg C, Clemenson GDJr., Fragniere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH, Bussey TJ. 2009. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325: 210-213.
13. Dellu F, Mayo W, Cherkaoui J, Le Moal M, Simon H. 1992. A two-trial memory task with automated recording: Study in young and aged rats. Brain Res 588: 132-139.
14. Deng W, Aimone JB, Gage FH. 2010. New neurons and new memories: How does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 11: 339-350.
15. Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza PV, Abrous DN. 2003. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc Natl Acad Sci U S A 100: 14385-14390.
16. Dupret D, Revest JM, Koehl M, Ichas F, De Giorgi F, Costet P, Abrous DN, Piazza PV. 2008. Spatial relational memory requires hippocampal adult neurogenesis. PLoS One 3: e1959
17. Fletcher BR, Calhoun ME, Rapp PR, Shapiro ML. 2006. Fornix lesions decouple the induction of hippocampal arc transcription from behavior but not plasticity. J Neurosci 26: 1507-1515.
18. Gage FH, Dunnett SB, Björklund A. 1984. Spatial learning and motor deficits in aged rats. Neurobiol Aging 5: 43-48.
19. Gallagher M, Burwell R, Burchinal M. 1993. Severity of spatial learning impairment in aging, development of a learning index for performance in the Morris water maze. Behav Neurosci 107: 618-626.
20. Giorgi C, Yeo GW, Stone ME, Katz DB, Burge C, Turrigiano G, Moore MJ. 2007. The EJC factor eIF4AIII modulates synaptic strength and neuronal protein expression. Cell 130: 179-191.
21. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. 1999. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2: 260-265.
22. Greer PL, Hanayama R, Bloodgood BL, Mardinly AR, Lipton DM, Flavell SW, Kim TK, Griffith EC, Waldon Z, Maehr R, Ploegh HL, Chowdhury S, Worley PF, Steen J, Greenberg ME. 2010. The Angelman Syndrome protein Ube3A regulates synapse development by ubiquitinating arc. Cell 140: 704-716.
23. Guzowski JF, Lyford GL, Stevenson GD, Houston FP, McGaugh JL, Worley PF, Barnes CA. 2000. Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J Neurosci 20: 3993-4001.
24. Hastings NB, Gould E. 1999. Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol 413: 146-154.
25. Jessberger S, Kempermann G. 2003. Adult-born hippocampal neurons mature into activity-dependent responsiveness. Eur J Neurosci 18: 2707-2712.
26. Kee N, Teixeira CM, Wang AH, Frankland PW. 2007. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 10: 355-362.
27. Kempermann G. 2008. The neurogenic reserve hypothesis: What is adult hippocampal neurogenesis good for? Trends Neurosci 31: 163-169.
28. Kuhn HG, Dickinson-Anson H, Gage FH. 1996. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16: 2027-2033.
29. Marr D. 1971. Simple memory: A theory for archicortex. Philos Trans R Soc Lond B Biol Sci 262: 23-81.
30. Marrone DF, Adams AA, Satvat E. 2011. Increased pattern separation in the aged fascia dentata. Neurobiol Aging 32: 2317.
31. Marrone DF, Satvat E, Shaner MJ, Worley PF, Barnes CA. 2012. Attenuated long-term Arc expression in the aged fascia dentata. Neurobiol Aging 33: 979-990.
32. McHugh TJ, Jones MW, Quinn JJ, Balthasar N, Coppari R, Elmquist JK, Lowell BB, Fanselow MS, Wilson MA, Tonegawa S. 2007. Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317: 94-99.
33. McNaughton BL, Morris RGM. 1987. Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10: 408-415.
34. McNaughton BL, Nadel L. 1990. Hebb-Marr networks and the neurobiological representation of action in space. In: Gluck MA, Rumelhart DE, editors. Neuroscience and Connectionist Theory. Hillsdale: Lawrence Erlbaum Associates. pp 1-63.
35. Montaron MF, Drapeau E, Dupret D, Kitchener P, Aurousseau C, Le Moal M, Piazza PV, Abrous DN. 2006. Lifelong corticosterone level determines age-related decline in neurogenesis and memory. Neurobiol Aging 27: 645-654.
36. Morris RG, Garrud P, Rawlins JN, O'Keefe J. 1982. Place navigation impaired in rats with hippocampal lesions. Nature 297: 681-683.
37. Niewoehner B, Single FN, Hvalby Ø, Jensen V, Meyer zum Alten Borgloh S, Seeburg PH, Rawlins JN, Sprengel R, Bannerman DM. 2007. Impaired spatial working memory but spared spatial reference memory following functional loss of NMDA receptors in the dentate gyrus. Eur J Neurosci 25: 837-846.
38. O'Reilly RC, McClelland JL. 1994. Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off. Hippocampus 4: 661-682.
39. Panja D, Dagyte G, Bidinosti M, Wibrand K, Kristiansen AM, Sonenberg N, Bramham CR. 2009. Novel translational control in Arc-dependent long term potentiation consolidation in vivo. J Biol Chem 284: 31498-31511.
40. Penner MR, Roth TL, Chawla MK, Hoang LT, Roth ED, Lubin FD, Sweatt JD, Worley PF, Barnes CA. 2011. Age-related changes in Arc transcription and DNA methylation within the hippocampus. Neurobiol Aging 32: 2198-2210.
41. Peters A, Rosene DL, Moss MB, Kemper TL, Abraham CR, Tigges J, Albert MS. 1996. Neurobiological bases of age-related cognitive decline in the rhesus monkey. J Neuropathol Exp Neurol 55: 861-874.
42. Plath N, Ohana O, Dammermann B, Errington ML, Schmitz D, Gross C, Mao X, Engelsberg A, Mahlke C, Welzl H, Kobalz U, Stawrakakis A, Fernandez E, Waltereit R, Bick-Sander A, Therstappen E, Cooke SF, Blanquet V, Wurst W, Salmen B, Bösl MR, Lipp H-P, Grant SGN, Bliss TVP, Wolfer DP, Kuhl D. 2006. Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52: 437-444.
43. Ramirez-Amaya V, Vazdarjanova A, Mikhael D, Rosi S, Worley PF, Barnes CA. 2005. Spatial exploration-induced Arc mRNA and protein expression: Evidence for selective, network-specific reactivation. J Neurosci 25: 1761-1768.
44. Ramirez-Amaya V, Marrone DF, Gage FH, Worley PF, Barnes CA. 2006. Integration of new neurons into functional neural networks. J Neurosci 26: 12237-12241.
45. Rao MS, Hattiangady B, Abdel-Rahman A, Stanley DP, Shetty AK. 2005. Newly born cells in the ageing dentate gyrus display normal migration, survival and neuronal fate choice but endure retarded early maturation. Eur J Neurosci 21: 464-476.
46. Rapp PR, Gallagher M. 1996. Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc Natl Acad Science USA 93: 9926-9930.
47. Rasmussen T, Schliemann T, Sorensen JC, Zimmer J, West MJ. 1996. Memory impaired aged rats: No loss of principal hippocampal and subicular neurons. Neurobiol Aging 17: 1443-1447.
48. Rosenzweig ES, Rao G, McNaughton BL, Barnes CA. 1997. Role of temporal summation in age-related long-term potentiation-induction deficits. Hippocampus 7: 549-558.
49. Sandoval CJ, Martinez-Claros M, Bello-Medina PC, Pérez O, Ramirez-Amaya V. 2011. When are new hippocampal neurons, born in the adult brain, integrated into the network that processes spatial information? PLoS One 6: e17689
50. Seki T, Arai Y. 1995. Age-related production of new granule cells in the adult dentate gyrus. Neuroreport 6: 2479-2482.
51. Shen J, Barnes CA. 1996. Age-related decrease in cholinergic synaptic transmission in three hippocampal subfields. Neurobiol Aging 17: 439-451.
52. Shen J, Barnes CA, Wenk GL, McNaughton BL. 1996. Differential effects of selective immunotoxic lesions of medial septal cholinergic cells on spatial working and reference memory. Behav Neurosci 110: 1181-1186.
53. Small SA, Chawla MK, Buonocore M, Rapp PR, Barnes CA. 2004. Imaging correlates of brain function in monkeys and rats isolates a hippocampal subregion differentially vulnerable to aging. Proc Natl Acad Sci USA 101: 7181-7186.
54. Snyder JS, Choe JS, Clifford MA, Jeurling SI, Hurley P, Brown A, Kamhi JF, Cameron HA. 2009. Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J Neurosci 29: 14484-14495.
55. Song HJ, Stevens CF, Gage FH. 2002. Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat Neurosci 5: 438-445.
56. Stanfield BB, Trice JE. 1988. Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections. Exp Brain Res 72: 399-406.
57. Stark SM, Yassa MA, Stark CE. 2010. Individual differences in spatial pattern separation performance associated with healthy aging in humans. Learn Mem 17: 284-288.
58. Stone SS, Teixeira CM, Zaslavsky K, Wheeler AL, Martinez-Canabal A, Wang AH, Sakaguchi M, Lozano AM, Frankland PW. 2011. Functional convergence of developmentally and adult-generated granule cells in dentate gyrus circuits supporting hippocampus-dependent memory. Hippocampus 21: 1348-1362.
59. Taghzouti K, Léna I, Dellu F, Roques BP, Daugé V, Simon H. 1999. Cognitive enhancing effects in young and old rats of pBC264, a selective CCKB receptor agonist. Psychopharmacology (Berl) 143: 141-149.
60. Tashiro A, Makino H, Gage FH. 2007. Experience-specific functional modification of the dentate gyrus through adult neurogenesis: A critical period during an immature stage. J Neurosci 27: 3252-3259.
61. Treves A, Rolls ET. 1992. Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus 2: 189-199.
62. van Praag H, Kempermann G, Gage FH. 1999. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2: 266-270.
63. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH. 2002. Functional neurogenesis in the adult hippocampus. Nature 415: 1030-1034.
64. West MJ. 1993. Regionally specific loss of neurons in the aging human hippocampus. Neurobiol Aging 14: 287-293.
65. West MJ, Amaral DJ, Rapp PR. 1993. Preserved hippocampal cell number in aged monkeys with recognition memory deficits. Soc Neurosci Abstr 19: 599
66. Wiskott L, Rasch MJ, Kempermann G. 2006. A functional hypothesis for adult hippocampal neurogenesis: Avoidance of catastrophic interference in the dentate gyrus. Hippocampus 16: 329-343.
67. Yassa MA, Lacy JW, Stark SM, Albert MS, Gallagher M, Stark CE. 2011. Pattern separation deficits associated with increased hippocampal CA3 and dentate gyrus activity in nondemented older adults. Hippocampus 21: 968-979.